Avian wings can lengthen rather than shorten in response to increased migratory predation danger

Abstract Increasing predation danger can select for safety‐enhancing modifications to prey morphology. Here, we document the multi‐decade wing lengthening of a Pacific flyway migrant, the western sandpiper (Calidris mauri), and contrast this with contemporaneous wing shortening of the closely related semipalmated sandpiper (C. pusilla) on the Atlantic flyway. We measured >12,000 southbound western sandpipers captured from 1978 to 2020 at a major stopover site in British Columbia. Wing length increased at 0.074 mm year−1 (SE = 0.017; p < .0003) for adults, and 0.087 mm year−1 (SE = 0.029; p < .007) for juveniles. These rates are of similarly large magnitude (4%–5% overall), but opposite in direction, to the rate we previously reported for semipalmated sandpiper adults (−0.103 mm year−1). In both species, the change is specific to wings rather than being part of a general body size change. We interpret both trends as responses to the ongoing strong increase of peregrine falcon (Falco peregrinus) populations since the mid‐1970s, an important predator encountered by these species in contrasting ways during migration. Western sandpipers and peregrine migrations have temporal and spatial overlap. Longer wings enhance migratory speed and efficiency, enabling western sandpipers to decrease overlap by advancing to safer zones ahead of falcon passage. In contrast, semipalmated sandpipers primarily encounter peregrines as residents at migratory staging sites. Shorter wings improve acceleration and agility, helping migrants to escape attacks. Juvenile western sandpiper wing length also shows a component additive to the lengthening trend, shifting between years at 0.055 mm day−1 with the highly variable snowmelt date, with wings shorter following early springs. On the Pacific flyway, the timing of peregrine southward passage advances with snowmelt, increasing the relative exposure of juveniles to post‐migratory resident peregrines. We interpret this annual wing length adjustment as an induced defense, made possible because snowmelt timing is a reliable cue to danger in the upcoming migration.

than being part of a general body size change. We interpret both trends as responses to the ongoing strong increase of peregrine falcon (Falco peregrinus) populations since the mid-1970s, an important predator encountered by these species in contrasting ways during migration. Western sandpipers and peregrine migrations have temporal and spatial overlap. Longer wings enhance migratory speed and efficiency, enabling western sandpipers to decrease overlap by advancing to safer zones ahead of falcon passage. In contrast, semipalmated sandpipers primarily encounter peregrines as residents at migratory staging sites. Shorter wings improve acceleration and agility, helping migrants to escape attacks. Juvenile western sandpiper wing length also shows a component additive to the lengthening trend, shifting between years at 0.055 mm day −1 with the highly variable snowmelt date, with wings shorter following early springs. On the Pacific flyway, the timing of peregrine southward passage advances with snowmelt, increasing the relative exposure of juveniles to post-migratory resident peregrines. We interpret this annual wing length adjustment as an induced defense, made possible because snowmelt timing is a reliable cue to danger in the upcoming migration.

K E Y W O R D S
migration, morphology, peregrine falcon, predation danger, sandpipers, wing shape

| INTRODUC TI ON
Experiments in micro-and mesocosms demonstrate that an increase in the presence of predators can lead to safety-enhancing changes in the behavior and morphology of prey (Brönmark & Miner, 1992;Hoverman et al., 2005;McCollum & Leimberger, 1997;Oufiero et al., 2011). These experiments demonstrate both rapid microevolutionary and phenotypically plastic responses (O'Steen et al., 2002;Reznick et al., 1990). Field studies (DeWitt et al., 2019;Hammerschlag et al., 2018) have documented findings consistent with these results, though experimental verification at a large scale in nature is more difficult to acquire (Sheriff et al., 2020). Here we consider the hypothesis that ongoing wing length changes of two migratory sandpiper species are safety-enhancing responses to raptor population recovery.
Many papers describe animal morphological change over recent decades, including at least 12 papers documenting long-term directional changes in the wing length of bird species (Table 1). Climate change is invoked as the causal factor in some of these studies (1-5 in Table 1). Others (6-10 in Table 1) invoke changing environmental demands on flight performance attributes. Flight speed, power requirement, acceleration, climb rate, agility, and energy efficiency are all strongly influenced by wing morphology (Pennycuick, 1989).
A change in the relative importance of these performance characteristics in any type of flight (foraging, display, migration, predator escape; Marchetti et al., 1995) would exert corresponding selection pressure on wing morphology. Examples include large-scale habitat change requiring more or less flight (Desrochers, 2010), altered migration routing or timing requiring more extended or faster travel (Hahn et al., 2016), and changed predator abundance that alters the importance of escape ability.
This study focuses on wing morphology with respect to migration and predation danger. Wing shape embodies a trade-off between traits that improve long-distance flight performance against those that improve predator escape ability (Hahn et al., 2016;Phillips et al., 2018). Relatively long, pointed, and concave wings have less drag and are more energy efficient, thus supporting faster overall migratory progression (distance per day). In contrast, relatively short, round, and convex wings provide more lift, acceleration, and agility, thus improving escape performance during predator attacks (Burns, 2003;Hedenström & Møller, 1992;Pennycuick et al., 1994;Swaddle & Lockwood, 1998;Vágási et al., 2016).
The selective balance of defensive attributes can shift with predator population size. Gosler et al. (1995) investigated multi-decade changes in the mid-winter body mass of the great tit (Parus major) in England in relation to changes in predator abundance, based on the idea that greater body mass (due to extra fat) reduces starvation but raises predation risk. Mid-winter body mass rose as sparrowhawk (Accipiter nisus) populations were decimated by intense DDT usage beginning in the late 1940s, and then fell in the 1970s as sparrowhawk populations recovered.
Raptor numbers in North America followed a similar trajectory.
Peregrines (Falco peregrinus) were threatened with extirpation over large parts of their range until the mid-1970s, when the decline reversed following DDT regulation, the enactment of endangered species legislation, and the initiation of many conservation measures, including introductions of captive-bred birds into the wild. These steps proved effective and the peregrine was removed from the U.S. endangered species list in 1999 (Cade & Burnham, 2003). Other raptor species have also increased since the mid-1970s, and the ongoing upward trend of raptor numbers in North America contrasts strongly with the declines of most other groups of birds (Rosenberg et al., 2019). Lank et al. (2017) considered the effect of steadily climbing peregrine numbers on the wing size and shape of migratory semipalmated sandpipers (Calidris pusilla), assuming that shorter, rounder wings to facilitate escape would be increasingly favored. They show that adult wings shortened by ~3.8 mm from 1980 to 2015.
The change cannot be accounted for by greater declines of largerbodied eastern populations of this species (Bliss et al., 2019), as had originally been conjectured (Hicklin & Chardine, 2012). An independent study documents similar wing shortening in two other long-distance Atlantic flyway migrant sandpiper species, as well as for juvenile semipalmated sandpipers (Anderson et al., 2019). Brown and Brown (2013) earlier proposed a similar hypothesis to explain wing shortening in the cliff swallow (Petrochelidon pyrrhonota), conjecturing that increased danger from road traffic selected for shorter wings because they provide greater agility and higher acceleration. Salewski, Hochachka, and Flinks (2014) list "increasing predation pressure" as a hypothesis potentially accounting for changing wing morphology of stonechats (Saxicola torquata) and note that this idea has yet to be tested.
Western sandpipers (Calidris mauri) have also experienced a large increase in the presence of peregrines along their migration route  Figure 1), though with a significant difference. On the Pacific flyway, peregrines and western sandpipers are co-migrants on both the northward and southbound migrations (Table 2; Ydenberg, 2022), with the temporal overlap especially large for southbound juveniles. On the Atlantic flyway, in contrast, semipalmated sandpipers have almost completed passage by the time migrant peregrines begin to arrive, and there is thus little southbound co-migration (Lank et al., 2003, Table 2). However, there are now populations of peregrine pairs breeding at each of their major southward migratory staging areas, populations established by the introduction of captive-bred peregrines in the 1980s (Dekker et al., 2011;Watts et al., 2015). These peregrines begin breeding before the  et al., 2022). Temporal overlap with migrating peregrines can be reduced by higher migratory speed (Hope et al., 2011(Hope et al., , 2014Ydenberg, 2022;Ydenberg et al., 2007), and also by earlier migratory departure (Jamieson et al., 2014). Sandpipers have up to twice the migratory speed of peregrines (~400 vs. 200 km day −1 ; Hope et al., 2011), so are able to reduce their exposure by advancing more quickly into lower danger zones ahead of migrant peregrines (Ydenberg & Hope, 2019 (1974Hope et al., 2020), altered space use (Sprague et al., 2008), and flocking behavior (e.g., Beauchamp, 2008Beauchamp, , 2016Beauchamp & Ruxton, 2008), and have taken up cliff roosting (MacKinnon et al., 2008) and over-ocean flocking (Dekker et al., 2011) in place of roosting on mudflats at high tide. Lank et al. (2017) suggested that wing shortening be added to this list of anti-predator adaptations.
Here we hypothesize that increasing peregrine populations select either for better escape performance (shorter, rounder, convex wings) or increased migratory speed (longer, pointed, concave wings), depending on the balance of danger posed by exposure to resident versus migratory falcons. Increasing peregrine numbers have made greater migratory speed advantageous on the Pacific flyway, and the hypothesis thus predicts that western sandpipers should have evolved longer rather than shorter wings (Figure 2). TA B L E 1 Studies reporting a change in avian wing morphology over recent decades. An experiment manipulating the exposure of migrant sandpipers would be impossible on any temporal or spatial scale large enough to be meaningful. However, extensive inter-annual variation in peregrine migration timing on the Pacific flyway provides a largescale natural experiment. The median southward passage timing of peregrines in southern British Columbia varies annually by 54 days (Table 2), shifting with spring onset. Earlier spring increases the proportion of peregrine southward passage preceding that of western sandpipers. Later-passaging western sandpipers, particularly juveniles, increasingly encounter these peregrines as post-migration residents settled for the winter (Ydenberg, 2022). The earliness of spring thus shifts the balance of benefits from defense against comigrating (longer wings) toward resident peregrines (shorter wings).
Behavioral aspects of defense (e.g., vigilance, stopover site choice, rate, and extent of fueling) are quickly adjusted. Some morphological aspects of defense can also be readily modified (e.g., muscle mass; van den Hout et al., 2010), albeit not as rapidly as behavior. But wing morphology can be adjusted only once annually when flight feathers are grown. Adult western sandpipers do not molt until after southward migration is completed, but juveniles grow their wing feathers before their initial southward migration and could, in principle, tailor wing morphology in anticipation of the type of migratory danger. Changes to defensive morphology induced by (cues to) predator presence are known in many systems ("induced defenses"; Tollrian & Harvell, 1999). We emphasize that doing so does not require juveniles to experience predators directly: they have only to adjust wing growth contingent on a cue relevant to migratory predation danger.
The timing of spring onset provides such a cue (Ydenberg, 2022).
Spring onset is a marked and rapid event on the Arctic breeding grounds of shorebirds, widely measured by snowmelt (e.g., van Gils  Table 2 were collected in the Salish Sea and the Bay of Fundy. Peregrines breed across the continent and in Greenland, the great majority north of 55°, and migrate in late summer and autumn. The October 1 location of the "falcon front" (the point of peak passage; Worcester & Ydenberg, 2008) is shown (white line). Peregrine passage is much earlier on the Pacific coast, and its timing is much more variable among years than along the Atlantic coast. Western sandpipers (yellow) migrate from breeding areas in coastal Arctic Alaska, beginning with a jump over the Gulf of Alaska to the Pacific Northwest, thereby evading "marine" peregrines of the sub-species pealei. They progress southward to non-breeding areas along coastlines of the Gulf of Mexico, and Central and South America. This portion of their migration overlaps temporally and spatially with that of southbound peregrines. Their exposure to migrating versus post-migration resident peregrines varies greatly among years. Semipalmated sandpipers (brown) breed across the Arctic from Alaska to Quebec (dark shade), migrating southeast to major Atlantic coastal staging sites (Bay of Fundy, and Delmarva peninsula, with adjacent Delaware and Chesapeake Bays) where they prepare for the long crossing to non-breeding areas in South America. Their southward passage precedes that of northern-breeding migrant peregrines, but they are exposed during several weeks of staging to peregrines introduced during the 1980s and now resident and breeding at these sites.
experimentally exposing great tit mothers to predators during laying altered levels of maternal steroids in the egg yolk, which in turn affected the growth and behavior of offspring-including the growth of longer wings.
We predict, therefore, that superimposed on the lengthening trend of wings, there is an additive component adjusting the annual mean wing length of juvenile (but not adult) western sandpipers, in direct relation to the date of spring onset. This mechanism favors shorter wings when spring is earlier due to the greater relative exposure to resident peregrines, and longer wings following later springs when relatively more exposure to co-migrating peregrines is expected.

| ME THODS
We measured wing ( To assess the relationship between wing length and shape, we quantified shape as the second size-constrained component (C2; Swaddle & Lockwood, 1998) (2010) in the Bay of Fundy (Dekker et al., 2011) and even more in Chesapeake Bay (Watts et al., 2015). b "Arrival" defined as the d-o-y on which 50% of the total passage was reached. The inter-annual average date is given. Based on Worcester and Ydenberg (2008). c Inter-annual range (in days) of peregrine arrival dates, based on Niehaus and Ydenberg (2006) for the Salish Sea, and the Bay of Fundy on an analysis of data from nearby North American Hawkwatch sites by Hong Ho (unpubl. report). d Median passage date varies little between years. Based on Lank et al. (2003), and Niehaus and Ydenberg (2006). e "Headstart" is the difference ( trends separately. Since there were no regional differences in slopes, we here produce a single trend line by adjusting the mean values for regional size differences with an ANOVA and modeling the adjusted wing lengths as a linear function of year.
We assessed the relationship of annual mean western sandpiper wing length to spring onset timing, based on snowmelt in western sandpiper breeding areas, following the method described by van

| RE SULTS
Intraspecific morphological variation of western and semipalmated sandpiper wings is similar and lies along an axis ranging from relatively

F I G U R E 2
We hypothesize that the selection on wing morphology for long-distance migrant sandpipers is generated by the relative exposure to resident versus co-migrating peregrines (horizontal axis). Wing morphology (vertical axis) ranges from short-rounded (more acceleration and agility) to long-pointed (more efficient in long-distance flight). Peregrines are important predators, with strong population recovery ongoing since ~1975. Wing morphology effective at countering this rising danger depends on whether migratory risk is better reduced by escape from attacks at staging sites (#1; semipalmated sandpipers, Atlantic flyway), or by outpacing peregrine migration between stopovers along the route (#2; western sandpipers, Pacific flyway). Relative exposure for western sandpipers also varies between years in direct relation to the variable onset of spring. Accordingly, juvenile wings (grown just prior to migration) are shorter in early spring years, and longer in late spring years (#3). This phenotypic plasticity, superimposed on the long-term lengthening trend, is interpreted as an induced defense.
short-and-rounded to relatively long-and-pointed wings (Figure 3).
The flattened, straightened wing length, therefore, provides a reasonable measure representing wing size and shape for both species.
Wing length (annual means, controlling for gender) of west- in 15 years), and 0.12 mm year −1 for juveniles (n = 7263 wings, 18 years). In contrast, adult semipalmated sandpiper wing length decreased  at an overall rate estimated at −0.103 mm year −1 (SE = 0.016, p < .0001, Figure 4). Over the decades, these produced 4-5% changes. In contrast, the rates of change in annual mean bill lengths of both species are statistically indistinguishable from zero (Table 3). Thus in neither species can the change in wing length be explained as part of a general response correlated with overall body size change.
The relationship between snowmelt date and juvenile western sandpiper annual residual mean wing length is portrayed in Figure 5.
Controlling for the long-term trend, snowmelt date shows the predicted effect, with residual juvenile wing length negative in years with early spring onset and positive when later. A model predicting juvenile wing length (annual mean gender-controlled residual) as a linear function of year and snowmelt date estimates that wings are shorter by 0.055 mm for each day that snowmelt is earlier (r 2 = .38, p = .008). No such effect is detectable for adults (r 2 = .08, p = .32).
The analogous model for culmen length shows no effect for either age class (p-values > .20).

TA B L E 3
The rate of change in mean annual wing and bill lengths (mm year −1 ) of adult (n = 23 years) and juvenile (n = 22 years) southbound migrant western sandpipers captured and measured on the Fraser estuary, British Columbia, between 1978 and 2020.

| DISCUSS ION
The data presented here show that the wings of western sandpipers lengthened steadily and substantially between 1978 and 2020, coincident with the recovery of peregrine falcon population numbers following the mid-1970s regulation of DDT. Wing length of the ecologically-similar semipalmated sandpiper shortened by about the same amount during this period . Based on measurements of 137 museum specimens collected prior to the mid-1970s, Lank et al. (2017) also showed that semipalmated sandpiper wings lengthened after DDT came into widespread usage, reaching a maximum in 1980, before beginning to shorten (Figure 4). They argued that as peregrine populations were decimated, escape performance declined in importance relative to flight performance. The effect of changes of this magnitude on flight performance is substantial: based on Program Flight (Version 1.14; Pennycuick, 1989), an increase in wing length of 4 mm adds ~25% to the flight range of a 25 g male western sandpiper.
Note that the absolute rates of change measured in western and semipalmated sandpipers (0.074-0.110 mm year −1 ) are at least an order of magnitude larger than those reported in other studies of wing length change (see Table 1), which range from ~0.001 to 0.005 mm year −1 . However, when expressed as "allochronic" phenotypic rates of change (estimated at 990 and 1100 darwins, for western and semipalmated sandpipers, respectively), they fall within the range of other studies reporting the impact of predators on morphology (Hendry & Kinnison, 1998).
In addition to documenting decade-scale changes in wing lengths, we tested the hypothesis that wing length changes are re- in the degree of temporal migratory overlap (Ydenberg, 2022). This creates an annually-repeated large-scale natural experiment (Barley & Meeuwig, 2017) with which to challenge the "co-migrating vs. resident predator" hypothesis. In years with an early spring, peregrine migration is well underway as western sandpipers depart breeding areas. This shifts their relative exposure away from co-migrants toward post-migratory peregrines that take up winter residency along the Pacific flyway (Ydenberg, 2022).
Juvenile western sandpipers grow wings just before their southward migration, and as predicted (Figure 1), the residual (relative to the lengthening inter-annual trend) annual mean wing length changes in direct relation to snowmelt date ( Figure 5). Our measures were made at the first major migratory stopover, and there is little exposure to peregrines or other predators along the route prior to this point . The changes in residual wing lengths can therefore not be attributed to direct killing and must have arisen prior to embarking on migration.
The ecology of juvenile western sandpipers shows pertinent features parallel to that of crucian carp Carassius carassius, a model system for the study of induced defenses (Tollrian & Harvell, 1999  . The points are residuals of expected annual means from a model with year as a linear term and controlled for gender. The effect of snowmelt date is thus additive to the lengthening effect of the year, with wing length shortening significantly by 0.055 mm for each day that snowmelt is earlier (r 2 = .38, p = .008).
Recent interest in climate change has stimulated an extensive literature interpreting patterns of morphological change as thermoregulatory responses to higher ambient temperature (e.g., Gardner et al., 2011Gardner et al., , 2014; see also Baudron et al., 2014;Rode et al., 2010;Weeks et al., 2019). Wings generally have no thermoregulatory function in birds (Swaddle & Lockwood, 1998), so studies invoking climate change as the cause (studies 1-5 in Table 1)  General body size change could result from size selection by predators, or be due to its effects on availability, vulnerability, or escape performance (Andraso & Barron, 1995;Domenici et al., 2008;McCollum & Leimberger, 1997;O'Steen et al., 2002;Reimchen, 1994;Reimchen & Nosil, 2004;Reznick et al., 1990). General body size change could also arise as a by-product of behavioral or physiological changes made to increase (or lower) safety in ways that also affect growth rates, such as more (less) cautious foraging (e.g., DeWitt et al., 2019) or a habitat shift (e.g., Swain et al., 2015). However, we could detect no change in another structural measure of body size (bill length) in either species, as would be expected if the change in wing length were attributable to general body size change. We also note that the interval between the hatch date of juvenile western sandpipers and their southward passage on the Fraser estuary (on average 54.3 ± 3.6 days) lengthens when the hatch is earlier (Niehaus & Ydenberg, 2006), suggesting that the growth period is if anything longer in early snowmelt years. Nonetheless wing lengths are shorter, opposite to what would be expected if the inter-annual variability resulted from a temporal constraint on primary feather growth prior to migratory departure.
In conclusion, we attribute the extensive and rapid changes in opposing directions of sandpiper species' wing lengths recorded since ~1980 to heightened migratory danger posed by the ongoing recovery of peregrine falcons. The changes seem likely to be due to selection on wing size and shape, both of which strongly affect flight performance attributes. That phenotypic plasticity also plays a role is suggested by the annual change in the (residual) wing length of juvenile western sandpipers, consistent with defensive morphology induced by cues to the relative exposure during migration to resident versus co-migrating peregrines. The fundamental trade-off in wing morphology pits energetic efficiency (enhanced by longer, pointier, concave wings) against flight performance attributes such as acceleration and agility (enhanced by shorter, rounder, convex wings).
The rate and direction of wing length change is due to changes in the relative importance of flight performance attributes as predator abundance climbed. Raptor species other than peregrines have also shown substantial increases in abundance since the mid-1970s, a trend that contrasts strongly with the decline shown by most other groups of birds in North America (Rosenberg et al., 2019). For many prey species, therefore, the past half-century spans a period of steadily increasing danger, suggesting that the hypothesis developed here could apply more broadly. writing -original draft (equal); writing -review and editing (equal).

ACK N OWLED G M ENTS
We

A PPE N D I X B WING LENGTH MEASUREMENT ERROR
During the review process, several referees commented that the measurement error is large, and raised the possibility that the changes we report are spurious. In this Appendix, we enlarge on the analysis of measurement error included in our previous paper on semipalmated sandpiper wing length change (Lank et al., 2017, p. 3251) for which a similar concern was raised.
Wings were measured to the nearest 1.0 mm (0.5 mm at some sites), and multiple observers contributed measures to both the semipalmated  and western sandpiper (this paper) studies. Measurement error for semipalmated sandpiper wings was assessed using data on 17,035 birds captured at James Bay, with measures made by 10 different observers 1975-1982 (368-2453 birds/observer/year). The mean deviation of each observer from the global mean was calculated: seven of the 10 observers fall within 0.5 mm of the global mean. The mean difference between the 45 possible pairs of observers is 0.53 mm (maximum difference 1.6 mm).
Independent measures of the same bird within a single season (n = 35) were used to estimate the intraclass correlation coefficient (i.e., repeatability, cf. Lessells & Boag, 1987). That value is 0.85. Lank et al. (2017) also report that substantial change was measured within sites despite having consistent investigator training, and even in one case when all birds were measured by a single observer. These assessments show though individual observers have consistent differences, their measures tend to lie close (within 1 mm)

Measurement error in western sandpipers
together, which is about equal to the accuracy of measurement. We conclude that measurement error is substantially less than the effect size. Moreover, most of the annual means reported in the papers are composed of measurements made by multiple individuals, whose individual biases would tend to offset rather than reinforce one another. Both studies show highly significant linear trends spanning 36-42 years, with data collected in many (>20 in each case) of the years, and overall change estimated at 3.5-4 mm, making it highly unlikely that the effect can be attributed to measurement biases or errors.
Finally, we point out again that the rates of wing length change measured in these two species (0.074-0.110 mm year −1 ) are at least an order of magnitude larger than those reported for other species in Table 1 (~0.001-0.005 mm year −1 ). As the basic measurement procedure and instruments are the same, the size of these rates can be expected to have made them easier to detect, and less likely to be attributable to measurement error.